PKB rescues calcineurin/NFAT-induced arrest of Rag expression and Pre-T cell differentiation

Journal of Immunology

Volumn 177, Issue 7, 2006, Pages 4567-4576

  Patra, Amiya K ^a   Drewes, Thomas ^b   Engelmann, Swen ^b   Chuvpilo, Sergei ^a   Kishi, Hiroyuki ^c   Hünig, Thomas ^a   Serfling, Edgar ^a   Bommhardt, Ursula H ^b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c UNIVERSITY OF TOYAMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; CALCINEURIN; CD2 ANTIGEN; CD27 ANTIGEN; CD5 ANTIGEN; CIS ACTING ELEMENT; CYCLOSPORIN A; HERMES ANTIGEN; INTERLEUKIN 2 RECEPTOR ALPHA; LIPOCORTIN 5; LUCIFERASE; MESSENGER RNA; PROTEIN BCL 2; PROTEIN KINASE B; PROTEIN P56; PROTEIN SERINE THREONINE KINASE; RAG1 PROTEIN; RAG2 PROTEIN; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; TRANSCRIPTION FACTOR NFAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CELL SUSPENSION; CHROMATIN IMMUNOPRECIPITATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENETIC TRANSFECTION; HISTOGRAM; LYMPHOCYTE DIFFERENTIATION; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGAN CULTURE; PHENOTYPE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T CELL LYMPHOMA; T LYMPHOCYTE; THYMOCYTE; THYMUS; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

EID: 33749117397     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.177.7.4567     Document Type: Article

References (82)

1. Sebzda, E., S. Mariathasan, T. Ohteki, R. Jones, M. F. Bachmann, and P. S. Ohashi. 1999. Selection of the T cell repertoire. Annu. Rev. Immunol. 17: 829-874.
2. Godfrey, D. I., and A. Zlotnik. 1993. Control points in early T-cell development. Immunol. Today 14: 547-553.
3. Wilson, A., W. Held, and H. R. MacDonald. 1994. Two waves of recombinase gene expression in developing thymocytes. J. Exp. Med. 179: 1355-1360.
4. Dudley, E. C., H. T. Petrie, L. M. Shah, M. J. Owen, and A. C. Hayday. 1994. T cell receptor β chain gene rearrangement and selection during thymocyte development in adult mice. Immunity 1: 83-93.
5. Kruisbeek, A. M., M. C. Haks, M. Carleton, A. M. Michie, J. C. Zúñiga-Pflücker, and D. L. Wiest. 2000. Branching out to gain control: how the pre-TCR is linked to multiple functions. Immunol. Today 21: 637-644.
6. Khor, B., and B. P. Sleckman. 2002. Allelic exclusion at the TCRβ locus. Curr. Opin. Immunol. 14: 230-234.
7. Michie, A. M., and J. C. Zúñiga-Pflücker. 2002. Regulation of thymocyte differentiation: pre-TCR signals and β-selection. Semin. Immunol. 14: 311-323.
8. Borowski, C., C. Martin, F. Gounari, L. Haughn, I. Aifantis, F. Grassi, and H. von Boehmer. 2002. On the brink of becoming a T cell. Curr. Opin. Immunol. 14: 200-206.
9. Rothenberg, E. V., and T. Taghon. 2005. Molecular genetics of T cell development. Annu. Rev. Immunol. 23: 601-649.
10. 2+ mobilization and activation of NF-κB and NFAT. Nat. Immunol. 2: 403-409.
11. Crabtree, G. R., and E. N. Olson. 2002. NFAT signaling: choreographing the social lives of cells. Cell 109(2 Suppl. 1): S67-S79.
12. 2+/calcineurin signalling in cells of the immune system. Biochem. Biophys. Res. Commun. 311: 1117-1132.
13. Liu, J., J. D. Farmer, Jr., W. S. Lane, J. Friedman, I. Weissman, and S. L. Schreiber. 1991. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66: 807-815.
14. Gao, E. K., D. Lo, R. Cheney, O. Kanagawa, and J. Sprent. 1988. Abnormal differentiation of thymocytes in mice treated with cyclosporin A. Nature 336: 176-179.
15. Jenkins, M. K., R. H. Schwartz, and D. M. Pardoll. 1988. Effects of cyclosporine A on T cell development and clonal deletion. Science 241: 1655-1658.
16. Holländer, G. A., D. A. Fruman, B. E. Bierer, and S. J. Burakoff. 1994. Disruption of T cell development and repertoire selection by calcineurin inhibition in vivo. Transplantation 58: 1037-1043.
17. + thymocytes undergoing thymic selection: requirement of calcineurin activation for thymic positive selection but not negative selection. J. Exp. Med. 181: 927-941.
18. Urdahl, K. B., D. M. Pardoll, and M. K. Jenkins. 1994. Cyclosporin A inhibits positive selection and delays negative selection in αβ TCR transgenic mice. J. Immunol. 152: 2853-2859.
19. + thymocyte negative selection. J. Immunol. 156: 4594-4601.
20. Bueno, O. F., E. B. Brandt, M. E. Rothenberg, and J. D. Molkentin. 2002. Defective T cell development and function in calcineurin A β-deficient mice. Proc. Natl. Acad. Sci. USA 99: 9398-9403.
21. Neilson, J. R., M. M. Winslow, E. M. Hur, and G. R. Crabtree. 2004. Calcineurin B1 is essential for positive but not negative selection during thymocyte development. Immunity 20: 255-266.
22. Hayden-Martinez, K., L. P. Kane, and S. M. Hedrick. 2000. Effects of a constitutively active form of calcineurin on T cell activation and thymic selection. J. Immunol. 165: 3713-3721.
23. Serfling, E., F. Berberich-Siebelt, S. Chuvpilo, E. Jankevics, S. Klein-Hessling, T. Twardzik, and A. Avots. 2000. The role of NF-AT transcription factors in T cell activation and differentiation. Biochim. Biophys. Acta 1498: 1-18.
24. Hogan, P. G., L. Chen, J. Nardone, and A. Rao. 2003. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 17: 2205-2232.
25. H cells. Nat. Immunol. 3: 48-54.
26. Chuvpilo, S., E. Jankevics, D. Tyrsin, A. Akimzhanov, D. Moroz, M. K. Jha, J. Schulze-Luehrmann, B. Santner-Nanan, E. Feoktistova, T. König, et al. 2002. Autoregulation of NFATc1/A expression facilitates effector T cells to escape from rapid apoptosis. Immunity 16: 881-895.
27. Adachi, S., Y. Amasaki, S. Miyatake, N. Arai, and M. Iwata. 2000. Successive expression and activation of NFAT family members during thymocyte differentiation. J. Biol. Chem. 275: 14708-14716.
28. Amasaki, Y., S. Miyatake, N. Arai, and K. Arai. 2000. Regulation of nuclear factor of activated T-cell family transcription factors during T-cell development in the thymus. J. Allergy Clin. Immunol. 106: S1-S9.
29. Yoshida, H., H. Nishina, H. Takimoto, L. E. Marengere, A. C. Wakeham, D. Bouchard, Y. Y. Kong, T. Ohteki, A. Shahinian, M. Bachmann, et al. 1998. The transcription factor NF-ATc1 regulates lymphocyte proliferation and Th2 cytokine production. Immunity 8: 115-124.
30. Schuh, K., B. Kneitz, J. Heyer, U. Bommhardt, E. Jankevics, F. Berberich-Siebelt, K. Pfeffer, H. K. Müller-Hermelink, A. Schimpl, and E. Serfling. 1998. Retarded thymic involution and massive germinal center formation in NF-ATp-deficient mice. Eur. J. Immunol. 28: 2456-2466.
31. Oukka, M., I.-C. Ho, F. C. de la Brousse, T. Hoey, M. J. Grusby, and L. H. Glimcher. 1998. The transcription factor NFAT4 is involved in the generation and survival of T cells. Immunity 9: 295-304.
32. Scheid, M. P., and J. R. Woodgett. 2001. PKB/AKT: functional insights from genetic models. Nat. Rev. Mol. Cell Biol. 2: 760-768.
33. Brazil, D. P., J. Park, and B. A. Hemmings. 2002. PKB binding proteins: getting in on the Akt. Cell 111: 293-303.
34. Yang, Z.-Z., O. Tschopp, A. Baudry, B. Dümmler, D. Hynx, and B. A. Hemmings. 2004. Physiological functions of protein kinase B/Akt. Biochem. Soc. Trans. 32(Pt. 2): 350-354.
35. Suzuki, A., M. T. Yamaguchi, T. Ohteki, T. Sasaki, T. Kaisho, Y. Kimura, R. Yoshida, A. Wakeham, T. Higuchi, M. Fukumoto, et al. 2001. T cell-specific loss of Pten leads to defects in central and peripheral tolerance. Immunity 14: 523-534.
36. Hagenbeek, T. J., M. Naspetti, F. Malergue, F. Garçon, J. A. Nunès, K. B. Cleutjens, J. Trapman, P. Krimpenfort, and H. Spits. 2004. The loss of PTEN allows TCR αβ lineage thymocytes to bypass IL-7 and pre-TCR-mediated signaling. J. Exp. Med. 200: 883-894.
37. Hinton, H. J., D. R. Alessi, and D. A. Cantrell. 2004. The serine kinase phosphoinositide-dependent kinase 1 (PDK1) regulates T cell development. Nat. Immunol. 5: 539-545.
38. Patra, A. K., S. Y. Na, and U. Bommhardt. 2004. Active protein kinase B regulates TCR responsiveness by modulating cytoplasmic-nuclear localization of NFAT and NF-κB proteins. J. Immunol. 172: 4812-4820.
39. Parsons, J. N., G. J. Wiederrecht, S. Salowe, J. J. Burbaum, L. L. Rokosz, R. L. Kincaid, and S. J. O'Keefe. 1994. Regulation of calcineurin phosphatase activity and interaction with the FK-506.FK-506 binding protein complex. J. Biol. Chem. 269: 19610-19616.
40. Weih, F., S. A. Lira, and R. Bravo. 1996. Overexpression of RelB in transgenic mice does not affect IκBα levels: differential regulation of RelA and RelB by the inhibitor protein. Oncogene 12: 445-449.
41. Na, S. Y., A. Patra, Y. Scheuring, A. Marx, M. Tolaini, D. Kioussis, B. Hemmings, T. Hünig, and U. Bommhardt. 2003. Constitutively active protein kinase B enhances Lck and Erk activities and influences thymocyte selection and activation. J. Immunol. 171: 1285-1296.
42. Hogquist, K. A., S. C. Jameson, W. R. Heath, J. L. Howard, M. J. Bevan, and F. R. Carbone. 1994. T cell receptor antagonist peptides induce positive selection. Cell 76: 17-27.
43. Wilson, A., and H. R. MacDonald. 1995. Expression of genes encoding the pre-TCR and CD3 complex during thymus development. Int. Immunol. 7: 1659-1664.
44. Kishi, H., X. C. Wei, Z. X. Jin, Y. Fujishiro, T. Nagata, T. Matsuda, and A. Muraguchi. 2000. Lineage-specific regulation of the murine RAG-2 promoter: GATA-3 in T cells and Pax-5 in B cells. Blood 95: 3845-3852.
45. Yannoutsos, N., V. Barreto, Z. Misulovin, A. Gazumyan, W. Yu, N. Rajewsky, B. R. Peixoto, T. Eisenreich, and M. C. Nussenzweig. 2004. A cis element in the recombination activating gene locus regulates gene expression by counteracting a distant silencer. Nat. Immunol. 5: 443-450.
46. Hsu, L. Y., J. Lauring, H. E. Liang, S. Greenbaum, D. Cado, Y. Zhuang, and M. S. Schlissel. 2003. A conserved transcriptional enhancer regulates RAG gene expression in developing B cells. Immunity 19: 105-117.
47. - murine thymocytes: in vivo developmental kinetics and T cell receptor β chain rearrangement status. J. Exp. Med. 177: 1079-1092.
48. Azzam, H. S., A. Grinberg, K. Lui, H. Shen, E. W. Shores, and P. E. Love. 1998. CD5 expression is developmentally regulated by T cell receptor (TCR) signals and TCR avidity. J. Exp. Med. 188: 2301-2311.
49. Gratiot-Deans, J., L. Ding, L. A. Turka, and G. Nunez. 1993. bcl-2 proto-oncogene expression during human T cell development: evidence for biphasic regulation. J. Immunol. 151: 83-91.
50. Hoffman, E. S., L. Passoni, T. Crompton, T. M. Leu, D. G. Schatz, A. Koff, M. J. Owen, and A. C. Hayday. 1996. Productive T-cell receptor β-chain gene rearrangement: coincident regulation of cell cycle and clonality during development in vivo. Genes Dev. 10: 948-962.
51. Taghon, T., M. A. Yui, R. Pant, R. A. Diamond, and E. V. Rothenberg. 2006. Developmental and molecular characterization of emerging β- and γδ-selected pre-T cells in the adult mouse thymus. Immunity 24: 53-64.
52. Hayday, A. C., D. F. Barber, N. Douglas, and E. S. Hoffman. 1999. Signals involved in γ/δ T cell versus α/β T cell lineage commitment. Semin. Immunol. 11: 239-249.
53. Haks, M. C., J. M. Lefebvre, J. P. Lauritsen, M. Carleton, M. Rhodes, T. Miyazaki, D. J. Kappes, and D. L. Wiest. 2005. Attenuation of γδTCR signaling efficiently diverts thymocytes to the αβ lineage. Immunity 22: 595-606.
54. Hayes, S. M., L. Li, and P. E. Love. 2005. TCR signal strength influences αβ/γδ lineage fate. Immunity 22: 583-593.
55. Oettinger, M. A., D. G. Schatz, C. Gorka, and D. Baltimore. 1990. RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J recombination. Science 248: 1517-1523.
56. Nicholson, K. M., and N. G. Anderson. 2002. The protein kinase B/Akt signalling pathway in human malignancy. Cell Signal 14: 381-395.
57. Malstrom, S., E. Tili, D. Kappes, J. D. Ceci, and P. N. Tsichlis. 2001. Tumor induction by an Lck-MyrAkt transgene is delayed by mechanisms controlling the size of the thymus. Proc. Natl. Acad. Sci. USA 98: 14967-14972.
58. Rathmell, J. C., R. L. Elstrom, R. M. Cinalli, and C. B. Thompson. 2003. Activated Akt promotes increased resting T cell size, CD28-independent T cell growth, and development of autoimmunity and lymphoma. Eur. J. Immunol. 33: 2223-2232.
59. Schlissel, M. S. 2003. Regulating antigen-receptor gene assembly. Nat. Rev. Immunol. 3: 890-899.
60. Jung, D., and F. W. Alt. 2004. Unraveling V(D)J recombination: insights into gene regulation. Cell 116: 299-311.
61. Baksh, S., H. R. Widlund, A. A. Frazer-Abel, J. Du, S. Fosmire, D. E. Fisher, J. A. DeCaprio, J. F. Modiano, and S. J. Burakoff. 2002. NFATc2-mediated repression of cyclin-dependent kinase 4 expression. Mol. Cell 10: 1071-1081.
62. Mandal, M., C. Borowski, T. Palomero, A. A. Ferrando, P. Oberdoerffer, F. Meng, A. Ruiz-Vela, M. Ciofani, J. C. Zúñiga-Pflücker, I. Screpanti, et al. 2005. The BCL2A1 gene as a pre-T cell receptor-induced regulator of thymocyte survival. J. Exp. Med. 201: 603-614.
63. Kawamura, T., K. Ono, T. Morimoto, M. Akao, E. Iwai-Kanai, H. Wada, N. Sowa, T. Kita, and K. Hasegawa. 2004. Endothelin-1-dependent nuclear factor of activated T lymphocyte signaling associates with transcriptional coactivator p300 in the activation of the B cell leukemia-2 promoter in cardiac myocytes. Circ. Res. 94: 1492-1499.
64. Wolfer, A., A. Wilson, M. Nemir, H. R. MacDonald, and F. Radtke. 2002. Inactivation of Notch1 impairs VDJβ rearrangement and allows pre-TCR-independent survival of early αβ lineage thymocytes. Immunity 16: 869-879.
65. Huang, E. Y., A. M. Gallegos, S. M. Richards, S. M. Lehar, and M. J. Bevan. 2003. Surface expression of Notch1 on thymocytes: correlation with the double-negative to double-positive transition. J. Immunol. 171: 2296-2304.
66. Ciofani, M., T. M. Schmitt, A. Ciofani, A. M. Michie, N. Cuburu, A. Aublin, J. L. Maryanski, and J. C. Zúñiga-Pfücker. 2004. Obligatory role for cooperative signaling by pre-TCR and Notch during thymocyte differentiation. J. Immunol. 172: 5230-5239.
67. Visan, I., J. S. Yuan, J. B. Tan, K. Cretegny, and C. J. Guidos. 2006. Regulation of intrathymic T-cell development by Lunatic Fringe- Notch1 interactions. Immunol. Rev. 209: 76-94.
68. Pai, S.-Y., M. L. Truitt, C.-N. Ting, J. M. Leiden, L. H. Glimcher, and I.-C. Ho. 2003. Critical roles for transcription factor GATA-3 in thymocyte development. Immunity 19: 863-875.
69. + stage. J. Immunol. 168: 1649-1658.
70. Voll, R. E., E. Jimi, R. S. Phillips, D. F. Barber, M. Rincon, A. C. Hayday, R. A. Flavell, and S. Ghosh. 2000. NF-κB activation by the pre-T cell receptor serves as a selective survival signal in T lymphocyte development. Immunity 13: 677-689.
71. Staal, F. J., F. Weerkamp, A. W. Langerak, R. W. Hendriks, and H. C. Clevers. 2001. Transcriptional control of T lymphocyte differentiation. Stem Cells 19: 165-179.
72. Ciofani, M., and J, C. Zúniga-Pflücker. 2005. Notch promotes survival of pre-T cells at the β-selection checkpoint by regulating cellular metabolism. Nat. Immunol. 6: 881-888.
73. Aifantis, I., J. Buer, H. von Boehmer, and O. Azogui. 1997. Essential role of the pre-T cell receptor in allelic exclusion of the T cell receptor β locus [Published erratum appears in 1997 Immunity 7: 895.] Immunity 7: 601-607.
74. Aifantis, I., V. I. Pivniouk, F. Gartner, J. Feinberg, W. Swat, F. W. Alt, H. von Boehmer, and R. S. Geha. 1999. Allelic exclusion of the T cell receptor β locus requires the SH2 domain-containing leukocyte protein (SLP)-76 adaptor protein. J. Exp. Med. 190: 1093-1102.
75. Marklund, U., K. Lightfoot, and D. Cantrell. 2003. Intracellular location and cell context-dependent function of protein kinase D. Immunity 19: 491-501.
76. Wang, Q. F., J. Lauring, and M. S. Schlissel. 2000. c-Myb binds to a sequence in the proximal region of the RAG-2 promoter and is essential for promoter activity in T-lineage cells. Mol. Cell Biol. 20: 9203-9211.
77. Verkoczy, L., D. Ait-Azzouzene, P. Skog, A. Martensson, J. Lang, B. Duong, and D. Nemazee. 2005. A role for nuclear factor κB/rel transcription factors in the regulation of the recombinase activator genes. Immunity 22: 519-531.
78. + T cells. Immunity 9: 637-647.
79. + T lymphocytes. Proc. Natl. Acad. Sci. USA 99: 15566-15571.
80. Vaitaitis, G. M., M. Poulin, R. J. Sanderson, K. Haskins, and D. H. Wagner, Jr. 2003. Cutting edge: CD40-induced expression of recombination activating gene (RAG)1 and RAG2: a mechanism for the generation of autoaggressive T cells in the periphery. J. Immunol. 170: 3455-3459.
81. Oettinger, M. A. 2004. How to keep V(D)J recombination under control. Immunol. Rev. 200: 165-181.
82. Wayne, J., H. Suh, Z. Misulovin, K. A. Sokol, K. Inaba, and M. C. Nussenzweig. 1994. A regulatory role for recombinase activating genes, RAG-1 and RAG-2, in T cell development. Immunity 1: 95-107.